Genetic accommodation and the role of ancestral plasticity in the evolution of insect eusociality

For over a century, biologists have proposed a role for phenotypic plasticity in evolution, providing an avenue for adaptation in addition to ‘mutation-first’ models of evolutionary change. According to the various versions of this idea, the ability of organisms to respond adaptively to their environment through phenotypic plasticity may lead to novel phenotypes that can be screened by natural selection. If these initially environmentally induced phenotypes increase fitness, then genetic accommodation can lead to allele frequency change, influencing the expression of those phenotypes. Despite the long history of ‘plasticity-first’ models, the importance of genetic accommodation in shaping evolutionary change has remained controversial – it is neither fully embraced nor completely discarded by most evolutionary biologists. We suggest that the lack of acceptance of genetic accommodation in some cases is related to a lack of information on its molecular mechanisms. However, recent reports of epigenetic transgenerational inheritance now provide a plausible mechanism through which genetic accommodation may act, and we review this research here. We also discuss current evidence supporting a role for genetic accommodation in the evolution of eusociality in social insects, which have long been models for studying the influence of the environment on phenotypic variation, and may be particularly good models for testing hypotheses related to genetic accommodation. Finally, we introduce ‘eusocial engineering’, a method by which novel social phenotypes are first induced by environmental modification and then studied mechanistically to understand how environmentally induced plasticity may lead to heritable changes in social behavior. We believe the time is right to incorporate genetic accommodation into models of the evolution of complex traits, armed with new molecular tools and a better understanding of non-genetic heritable elements.